Functional Outcomes in Children with Abusive Head Trauma Receiving Inpatient Rehabilitation Compared with Children with Nonabusive Head Trauma Sarah R. Risen, MD1,2, Stacy J. Suskauer, MD1,3,4, Ellen J. DeMatt5, Beth S. Slomine, PhD1,3,6, and Cynthia F. Salorio, PhD1,3,6 Objective To compare clinical features and functional outcomes of age- and sex-matched children with abusive and nonabusive head trauma receiving inpatient rehabilitation.
Study design Children with abusive head trauma (n = 28) and age- and sex-matched children with nonabusive head trauma (n = 20) admitted to an inpatient pediatric rehabilitation unit from 1995-2012 were studied. Acute hospitalization and inpatient rehabilitation records were retrospectively reviewed for pertinent clinical data: initial Glasgow Coma Scale score, signs of increased intracranial pressure, neuroimaging findings, and presence of associated injuries. Functional status at admission to and discharge from inpatient rehabilitation was assessed using the Functional Independence Measure for Children. Outcome at discharge and outpatient follow-up were described based on attainment of independent ambulation and expressive language. Results Children with abusive and nonabusive head trauma had similar levels of injury severity, although associated injuries were greater in those with abusive head trauma. Functional impairment upon admission to inpatient rehabilitation was comparable, and functional gains during inpatient rehabilitation were similar between groups. More children with nonabusive than with abusive head trauma attained independent ambulation and expressive language after discharge from rehabilitation; the difference was no longer significant when only children aged >12 months at injury were examined. There was variability in delay to obtain these skills and in the quality of gained skills in both groups. Conclusions Despite more associated injuries, children with abusive head trauma make significant functional gains during inpatient rehabilitation, comparable with an age- and sex-matched sample with nonabusive head trauma. Key functional skills may be gained by children in both groups following discharge from inpatient rehabilitation. (J Pediatr 2014;164:613-9).
A
busive head trauma is a common cause of pediatric traumatic brain injury (TBI).1 Compared with children with nonabusive head trauma, mortality and morbidity are consistently greater in children with abusive head trauma.2-4 Younger age at injury,5,6 more severe initial injuries,2,7-9 and higher rates of secondary injuries from hypoxia and/or ischemia2,8,10 may contribute to the worse outcomes observed after abusive head trauma. For survivors of abusive head trauma, the neurodevelopmental outcome is often considered to be globally poor, though closer examination reveals a range of outcomes, especially in functional skills. Barlow et al examined a number of outcome variables at follow-up (mean 59 months postinjury) in 25 children with abusive head trauma. Although 68% of the children had neurologic or cognitive abnormality at follow-up, 60% of children were reported to have normal functional mobility, and 64% had normal to mildly impaired speech and language function.11 On standardized testing evaluating neurocognitive development and adaptive behavior, Keenan et al demonstrated worse outcomes in children with abusive head trauma, who also accounted for a larger percentage of the reported clinical disabilities including speech delay or need for assistive mobility devices.4 Even though global outcome ratings are useful for broadly categorizing outcomes, they may not provide a clear picture of an individual’s functional skills. In discussions of prognosis after abusive head trauma, caregivers often ask questions about expectations for development of discrete skills that can improve quality of life, such as independent ambulation (IA) and expressive language (EL).
DFQ EL GCS IA ICP LOS TBI TTA WeeFIM
Developmental Functional Quotient Expressive language Glasgow Coma Scale Independent ambulation Intracranial pressure Length of stay in a rehabilitation facility Traumatic brain injury Time from injury to admission to inpatient rehabilitation (time of acute hospitalization) Functional Independence Measure for children
From the 1Kennedy Krieger Institute; Departments of 2 Neurology, 3Physical Medicine and Rehabilitation, and 4 Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD; 5VA Medical Center, Perry Point, MD; and 6Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD Funded by the Eunice Kennedy Shriver National Institute of Child Health and Development (K23HD061611 and T32HD007414-20). The authors declare no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2014 Mosby Inc. All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2013.10.075
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The need for inpatient rehabilitation is a marker for severity of injury, as it signifies the presence of substantial functional deficits at the end of the acute hospitalization. Interestingly, reports of the outcome of children with abusive head trauma admitted to inpatient rehabilitation are not available, though this is theoretically a group at high risk for poor outcomes. The purposes of this study were to compare clinical features of children with abusive head trauma admitted to an inpatient rehabilitation unit to ageand sex-matched children with nonabusive head trauma, to evaluate and compare functional changes during inpatient rehabilitation in children with abusive head trauma and nonabusive head trauma, and to evaluate and compare attainment of key skills (IA and EL) by children with abusive and nonabusive head trauma at discharge from inpatient rehabilitation and subsequent follow-up.
Methods This is a retrospective review of children with or without abusive head trauma receiving acute inpatient rehabilitation for brain injury at a single academically affiliated rehabilitation hospital from 1995-2012. The practice at this hospital is to admit children with even the lowest levels of function after acquired brain injury for the purpose of addressing goals such as caregiver training, tolerance to positioning, and management of irritability while observing for improvements in the child’s functional status. Children who had received inpatient rehabilitation at another facility prior to admission to this facility were not included. The Johns Hopkins Institutional Review Board granted approval for examination of data extracted from a clinical performance database and from review of medical records. Abusive Head Trauma Thirty-three patients with abusive head trauma were identified based on the International Classification of Diseases, Ninth Revision code 995 at the time of admission to inpatient rehabilitation. On record review, 28 of those patients had a diagnosis of abusive head trauma documented in acute care medical records (age range 2-51 months) and were included in analyses. A multidisciplinary child abuse team or maltreatment expert at a tertiary referral academic medical center confirmed the diagnosis of abusive head trauma in 19 children. For an additional 5 patients, the episode of abuse was either witnessed (2), the perpetrator confessed (2), or an arrest was made (1). The remaining 4 cases had a documented diagnosis of abusive head trauma, but the available medical records did not provide additional detail regarding how the diagnosis was reached. Nonabusive Head Trauma Age-matched patients with nonabusive TBI were identified by International Classification of Diseases, Ninth Revision code 854. Matches were chosen from admissions at any time from 1995-2012 based on closest matching age of injury 614
Vol. 164, No. 3 within 3 months. We additionally prioritized matches of the same sex and without weight-bearing restrictions from orthopedic injuries. Age-matched controls were available for 20 of the 28 patients with abusive head trauma (age range 2-53 months); there were no matches available for 7 of the 11 children with abusive head trauma at #9 months of age at injury. Of the 20 matched controls, 2 children had documented formal consultation by experts in abuse and maltreatment, who concluded that each injury was accidental. Three matches were of the opposite sex. One matched control had coexisting fractures but was cleared for full weight bearing 9 days after admission to rehabilitation (27 days prior to discharge). One potential match was excluded due to symptomatic late pseudoaneuryms thought to be unrelated to the injury. Mechanism of TBI among the matched controls was variable: 11 patients were involved in a motor vehicle accidents, and 7 of these patients were documented as properly restrained. Three children had a television fall on their head, and 1 was accidentally struck in the head with a horseshoe. Two children were struck by cars. The remaining 3 patients were involved in falls: one fall from a bed, another fall down concrete stairs, and a third fall from an approximately 12-foot-high window. Glasgow Coma Scale (GCS) was defined as the first documented GCS score.12 GCS was available for 19 of 28 patients with abusive head trauma and 18 of 20 patients with nonabusive head trauma. Significantly increased intracranial pressure (ICP) was defined as direct documentation of elevated ICP in those undergoing ICP monitoring, requirement for neurosurgical interventions to relieve increased ICP (craniotomy or craniectomy), or neuroimaging reports of cerebral herniation or extensive cerebral edema with midline shift. Placement of an ICP monitoring device alone was recorded but not included in this variable unless there was clear documentation of increased ICP. Neuroimaging findings were recorded from head computed tomography or brain magnetic resonance imaging reports or, if neuroimaging reports were unavailable (ie, for patients transferred from another institution), from documentation of results by a medical provider within admission or discharge records. All patients had head computed tomography results available, and brain magnetic resonance imaging reports were available for 18 children with abusive head trauma and 11 children with nonabusive head trauma. Presence was noted of subdural hematoma, epidural hematoma, subarachnoid hemorrhage, and intraparenchymal hemorrhage; the latter 3 were grouped as “other brain hemorrhage.” Presence of skull fracture was also noted. The following were considered risk factors for neurologic sequelae, which might affect the child’s outcome: acute cerebral infarction/ischemia as documented in neuroimaging reports or clinical records, cardiac arrest or apnea requiring intervention, and documentation of status epilepticus during the acute hospitalization. Retinal hemorrhage was evaluated by physician documentation of the presence or absence of unilateral or bilateral Risen et al
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March 2014 findings. Twenty-five of 28 children with abusive head trauma had ophthalmological reports. Of those with nonabusive head trauma, 8 children had documented ophthalmological evaluations, 5 to assess trauma-related conditions such as orbital roof fractures. Time from injury to admission to inpatient rehabilitation (time of acute hospitalization) (TTA) was calculated as the number of days from acute care admission to admission to inpatient rehabilitation. Length of stay in a rehabilitation facility (LOS) was defined as the number of days from inpatient rehabilitation admission to discharge. Functional Independence Measure for Children (WeeFIM) is an 18-item, performance-based instrument measuring functional skills in self-care, transportation/ locomotion, and communication/social domains. The WeeFIM provides an objective measure of a child’s functional abilities, grading performance on specific tasks on an ordinal scale of 1-7 reflecting increasing level of independence/reduced need for assistance. Full independence on all measures within the scale is expected by 7 years of age. Because the degree of independence on tasks is expected to depend on developmental age, WeeFIM scores are converted into a Developmental Functional Quotient (DFQ). WeeFIM DFQs describe a child’s functional skills as a percentage of those expected by age, based on a normative sample of WeeFIM scores.13-15 WeeFIM DFQs for self-care, mobility, cognition, and total function were collected as part of clinical care at admission to and discharge from rehabilitation. Given the limited WeeFIM skills evaluated during infancy, WeeFIM data were used only from children who were at least 1 year of age at the time of admission, yielding WeeFIM data for 17 of 28 patients with abusive head trauma and 16 of 20 patients with nonabusive head trauma. IA and EL were chosen as important qualitative functional outcomes. IA was defined as documentation of ambulation in daily living without assistance from another person. EL was defined as use of spoken words for communication. Documentation of IA and EL was available for all patients at discharge; however, at discharge, 11 patients in the abusive head trauma group and 4 patients in the nonabusive head trauma group were 12 months of age with abusive and nonabusive head trauma attained IA (59% vs 75%) and EL (59% vs 69%) by discharge from inpatient rehabilitation. Overall, 64% of children with abusive head trauma later gained IA, and a significantly higher percentage of children with nonabusive head trauma attained IA (95%) (P = .03). Ambulatory skills ranged from independent steps for inhome mobility to hemiplegic gait to age-appropriate community mobility and advanced gross motor skills. The median age of children who gained IA after discharge from rehabilitation was similar between groups (abusive head trauma: median age 26 months, range 14-30 months; nonabusive head trauma: median age 26 months, range 14-38 months). Additionally, IA was acquired, on average, 14 months after discharge (range 2-19 months) in children with abusive head trauma and 9 months (range 1-25 months) after discharge in the nonabusive head trauma cohort. Tables IV and V (available at www.jpeds.com) provide details on each patient including age at attainment of IA and EL and a description of function at the last available documentation (which ranged from the time of discharge to 16 years after discharge). EL skills ranged from single words used for basic communication to complete, fully articulated sentences and conversations. Although a higher percentage of children with nonabusive head trauma also attained EL (95%) compared with those with abusive head trauma (72%), this difference was not statistically significant (P = .11). EL was gained within a similar age range in both groups (abusive head trauma: median age 32.5 months, range 14-38 months; nonabusive head trauma: median age 26 months, range 14-48 months); Additionally, patients with abusive head trauma attained EL an average of 16 months after discharge from rehabilitation (range 7-31 months) compared with 7.4 months (range 1-25 months) in children with nonabusive head trauma. To evaluate the relationship between age at the time of injury and functional outcomes, group differences were examined in the subset of children aged $12 months at the
Table II. Change in mean WeeFIM DFQs from admission to discharge within and between groups* Abuse head trauma (n = 17)
Nonabusive head trauma (n = 16)
WeeFIM DFQ
Admission† DFQ
Dischargez DFQ
P value
Admission† DFQ
Discharge† DFQ
P value
Difference between groups over time, P value
Self-Care Mobility Communication Total
52 33 46 42
59 51 61 54
.053 .004 .016 .006
48 33 46 41
59 55 65 59
.007 .001 .001 .001
.355 .285 .267 .160
DFQ: (patient domain score/expected domain score per age) 100. *Children aged >12 months at the time of injury. †Difference in admission DFQs between groups is not statistically significant for any subset or total score. zDifference in discharge DFQs between groups is not statistically significant for any subset or total score.
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Table III. Attainment of IA and EL At discharge from rehabilitation (Excluding children aged £12 months at injury)
IA, No. EL, No.
Abusive head trauma (n = 17)
Nonabusive head trauma (n = 16)
P value
10 (59%) 10 (59%)
12 (75%) 11 (69%)
.47 .72
At follow-up evaluation* (Excluding children with insufficient follow-up documentation)
IA, No. EL, No.
Abusive head trauma (n = 25)
Nonabusive head trauma (n = 19)
16 (64%) 18 (72%)
18 (95%) 18 (95%)
.03 .11
At follow-up evaluation (Excluding children aged £12 months at injury and those with insufficient documentation) Abusive head trauma (n = 15)
Nonabusive head trauma (n = 16)
11 (73%) 13 (87%)
15 (94%) 15 (94%)
IA, No. EL, No.
.17 .60
*Age at which IA and EL gained, months to gain IA and EL, as well as descriptors of final outcome can be found in Tables IV and V.
time of injury, and there was no longer a significant betweengroup difference in attainment of IA (P = .17) or EL (P = .60). Furthermore, in examining overall functional outcomes independent of mechanism of injury, children who attained IA and EL were older at injury than were those who did not (P = .045 and P = .08, respectively). Children who experienced associated injuries were less likely to achieve IA (P = .027) than were those who did not have secondary neurological insults. No other demographic or injury related factors were related to follow-up outcome of IA or EL.
Discussion Children with abusive and nonabusive head trauma were similar with respect functional impairment at admission to inpatient rehabilitation and gains made during inpatient rehabilitation. This highlights the potential for children with abusive head trauma to make short-term functional gains and benefit from inpatient rehabilitation. The use of age- and sex-matched populations of children with abusive and nonabusive head trauma is important, as younger age at injury has been associated with worse neurodevelopmental outcome5,6 and sex may modify response to ischemic insults or brain injury.16,17 Although the groups were age matched overall, there were more children aged #9 months at injury within the abusive head trauma group, consistent with the higher rate of abusive head trauma in infants.18 The average age of children with abusive head trauma in our sample was 20 months, which is older than that in many prior reports.18,19 This may reflect our inclusion of children through 5 years of age and a bias toward fewer but more impaired infants in our inpatient rehabilitation sample, as infants with sufficient feedings skills are commonly discharged from acute care to a home setting. GCS scores and signs of increased ICP were similar between groups, reflecting similar injury acuity. Neuroimaging and retinal hemorrhage findings are consistent with current
understanding of abusive head trauma and suggest that our patients were appropriately categorized.20 Associated injuries with neurological impact were significantly more common in children with abusive head trauma; both ischemia/infarction and status epilepticus were 6 times more common in abusive head trauma, and cardiorespiratory arrest/apnea was 4 times more common in abusive head trauma. This is consistent with prior reports of ischemia/infarctions,8,10,21 cardiorespiratory arrest/apnea,2,22,23 and posttraumatic seizures6,24 occurring more frequently in abusive head trauma. Similar to prior reports correlating severity of injury with disability in children with TBI,2,4,19 the presence of associated injuries was associated with worse outcome in our sample. Distinguishing the independent contribution from mechanism and severity of injury on outcomes is difficult given the overlap in abusive head trauma and associated injuries. However, in our sample, there was no difference in TTA, indicating that duration of acute hospitalization was similar despite the increased associated injuries in children with abusive head trauma. Although not statistically significant, the longer LOS in rehabilitation for the children with abusive head trauma may reflect social factors associated with abusive head trauma, which can complicate discharge planning or may reflect that children with abusive head trauma need additional time to gain a similar degree of skills. Even though we were unable to examine quantitative functional gains during inpatient rehabilitation in children aged #12 months due to the lack of reliable standardized functional assessment tools for this population, we were able to assess the rate of achievement of IA and EL in children injured at all ages. More than 50% of children with abusive and nonabusive head trauma achieved these skills at the time of discharge from inpatient rehabilitation; as children admitted to inpatient rehabilitation typically do not have IA, this again highlights the opportunity for meaningful short-term functional gains from inpatient rehabilitation in children with brain injury.
Functional Outcomes in Children with Abusive Head Trauma Receiving Inpatient Rehabilitation Compared with Children with Nonabusive Head Trauma
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Almost all children with nonabusive head trauma attained IA and EL after discharge from inpatient rehabilitation, whereas two-thirds of children in the abusive head trauma group eventually gained IA and nearly three-fourths gained EL within 31 months from rehabilitation discharge. The discrepancy in functional outcomes between children with abusive and nonabusive head trauma has been previously reported in a younger cohort of children.2,4,8 Although the abilities to ambulate and communicate have important implications for a child and the family’s daily function, the quality of these skills was variable in this cohort. It is also important to note that children in both groups achieved IA and EL well beyond the developmentally expected age range and often >12 months from the time of discharge. This is consistent with prior reports of children attaining functional skills over several years after TBI.25 When our analysis of IA and EL was limited to children at least 12 months of age at injury, there was no longer a significant difference in between-group outcome at follow-up. This is consistent with prior studies identifying worse outcomes in younger children with TBI,5,6 though other studies have failed to find differences in outcome based on age.25-27 This finding may also reflect the bias of our sample toward the most impaired infants. Larger studies with a matched sample of the youngest children would be useful for assessing differences in outcomes for infants with TBI. Additional limitations of this study include small sample size with documentation ranging over a 17-year period from multiple providers although drawn from a single rehabilitation unit; even though this was necessary to achieve the relatively small sample size presented, it is possible that variations in care during that period could have influenced outcomes. As admission practices vary among rehabilitation institutes, our cohort may differ from those admitted for inpatient rehabilitation elsewhere. Although WeeFIM data represent quantitative data acquired prospectively as part of clinical care, the other data obtained through chart review are based on documentation that was occasionally incomplete. For instance, we were unable to evaluate long-term outcomes in cognition and behavior due to inconsistent documentation of these skills in the available records. We were also unable to gather complete data on family and socioeconomic factors that have also been shown to influence outcome after TBI in children.4,28 Future studies designed to prospectively collect outcome data in a standardized fashion across multiple centers would be useful for better understanding the range of outcomes after abusive head trauma. Combining such outcome data with updated acute evaluations, such as biological markers and advanced neuroimaging techniques, will be useful for improving prognostication shortly after injury. n Submitted for publication May 29, 2013; last revision received Sep 19, 2013; accepted Oct 28, 2013. Reprint requests: Stacy J. Suskauer, MD, 707 N Broadway, Baltimore, MD 21230. E-mail: [email protected]
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References 1. Parks S, Sugerman D, Xu L, Coronado V. Characteristics of non-fatal abusive head trauma among children in the USA, 2003-2008: application of the CDC operational case definition to national hospital inpatient data. Inj Prev 2012;18:392-8. 2. Hymel KP, Makoroff KL, Laskey AL, Conaway MR, Blackman JA. Mechanisms, clinical presentations, injuries, and outcomes from inflicted versus noninflicted head trauma during infancy: results of a prospective, multicentered, comparative study. Pediatrics 2007;119:922-9. 3. Minns RA, Jones PA, Barlow KM. Outcome and prognosis of nonaccidental head injury in infants. In: Minns RA, ed. Shaking and other nonaccidental head injuries in vhildren. London, UK: MacKeith Press; 2006. p. 364-414. 4. Keenan HT, Hooper SR, Wetherington CE, Nocera M, Runyan DK. Neurodevelopmental consequences of early traumatic brain injury in 3-year-old children. Pediatrics 2007;119:e616-23. 5. Duhaime AC, Christian C, Moss E, Seidl T. Long-term outcome in infants with the shaking-impact syndrome. Pediatr Neurosurg 1996;24: 292-8. 6. Kieslich M, Marquardt G, Galow G, Lorenz R, Jacobit G. Neurological and mental outcome after severe head injury in childhood: a longterm follow-up of 318 children. Disabil Rehabil 2001;23:665-9. 7. Adamo MA, Drazin D, Smith C, Waldman JB. Comparison of accidental and nonaccidental traumatic brain injuries in infants and toddlers: demographics, neurosurgical interventions, and outcomes. J Neurosurg Pediatr 2009;4:414-9. 8. Ewing-Cobbs L, Prasad M, Kramer L, Landry S. Inflicted traumatic brain injury: relationship of developmental outcome to severity of injury. Pediatr Neurosurg 1999;31:251-8. 9. Goldstein B, Kelly MM, Bruton D, Cox C. Inflicted versus accidental head injury in critically injured children. Crit Care Med 1993;21: 1328-32. 10. Ichord RN, Naim M, Pollock AN, Nance ML, Margulies SS, Christian CW. Hypoxic-ischemic injury complicates inflicted and accidental traumatic brain injury in young children: the role of diffusionweighted imaging. J Neurotrauma 2007;24:106-18. 11. Barlow KM, Thomson E, Johnson D, Minns RA. Late neurologic and cognitive sequelae of inflicted traumatic brain injury in infancy. Pediatrics 2005;116:e174-85. 12. Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet 1974;2:81-4. 13. Msall ME, Tremont MR. Measuring functional status in children with genetic impairments. Am J Med Genet 1999;89:62-74. 14. Ottenbacher KJ, Msall ME, Lyon N, Duffy LC, Ziviani J, Granger CV, et al. The WeeFIM instrument: its utility in detecting change in children with developmental disabilities. Arch Phys Med Rehabil 2000; 81:1317-26. 15. Uniform Data System for Medical Rehabilitation. The WeeFIM II Clinical Guide, Version 6.0. Buffalo, NY: UDSMR; 2006. 16. Morrison WE, Arbelaez JJ, Fackler JC, De Maio A, Paidas CN. Gender and age effects on outcome after pediatric traumatic brain injury. Pediatr Crit Care Med 2004;5:145-51. 17. Zhu C, Xu F, Wang X, Shibata M, Uchiyama Y, Blomgren K, et al. Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. J Neurochem 2006;96:1016-27. 18. Leventhal JM, Martin KD, Asnes AG. Fractures and traumatic brain injuries: abuse versus accidents in a US database of hospitalized children. Pediatrics 2010;126:e104-15. 19. Ewing-Cobbs L, Kramer L, Prasad M, Canales DN, Louis PT, Fletcher JM, et al. Neuroimaging, physical, and developmental findings after inflicted and noninflicted traumatic brain injury in young children. Pediatrics 1998;102:300-7. 20. Kemp AM, Jaspan T, Griffiths J, Stoodley N, Mann MK, Tempest V, et al. Neuroimaging: what neuroradiological features distinguish abusive from non-abusive head trauma? A systematic review. Arch Dis Child 2011;96:1103-12.
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March 2014 21. Squier W. The “Shaken Baby” syndrome: pathology and mechanisms. Acta Neuropathol 2011;122:519-42. 22. King WJ, MacKay M, Sirnick A. Shaken baby syndrome in Canada: clinical characteristics and outcomes of hospital cases. CMAJ 2003; 168:155-9. 23. Piteau SJ, Ward MG, Barrowman NJ, Plint AC. Clinical and radiographic characteristics associated with abusive and nonabusive head trauma: a systematic review. Pediatrics 2012;130: 315-23. 24. Greiner MV, Lawrence AP, Horn P, Newmeyer AJ, Makoroff KL. Early clinical indicators of developmental outcome in abusive head trauma. Childs Nerv Syst 2012;28:889-96.
ORIGINAL ARTICLES 25. Anderson V, Catroppa C, Godfrey C, Rosenfeld JV. Intellectual ability 10 years after traumatic brain injury in infancy and childhood: what predicts outcome? J Neurotrauma 2012;29:143-53. 26. Rhine T, Wade SL, Makoroff KL, Cassedy A, Michaud LJ. Clinical predictors of outcome following inflicted traumatic brain injury in children. J Trauma Acute Care Surg 2012;73:S248-53. 27. Ewing-Cobbs L, Fletcher JM, Levin HS, Francis DJ, Davidson K, Miner ME. Longitudinal neuropsychological outcome in infants and preschoolers with traumatic brain injury. J Int Neuropsychol Soc 1997;3:581-91. 28. Crowe LM, Catroppa C, Babl FE, Anderson V. Intellectual, behavioral, and social outcomes of accidental traumatic brain injury in early childhood. Pediatrics 2012;129:e262-8.
Functional Outcomes in Children with Abusive Head Trauma Receiving Inpatient Rehabilitation Compared with Children with Nonabusive Head Trauma
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12
N (
Study design Children with abusive head trauma (n = 28) and age- and sex-matched children with nonabusive head trauma (n = 20) admitted to an inpatient pediatric rehabilitation unit from 1995-2012 were studied. Acute hospitalization and inpatient rehabilitation records were retrospectively reviewed for pertinent clinical data: initial Glasgow Coma Scale score, signs of increased intracranial pressure, neuroimaging findings, and presence of associated injuries. Functional status at admission to and discharge from inpatient rehabilitation was assessed using the Functional Independence Measure for Children. Outcome at discharge and outpatient follow-up were described based on attainment of independent ambulation and expressive language. Results Children with abusive and nonabusive head trauma had similar levels of injury severity, although associated injuries were greater in those with abusive head trauma. Functional impairment upon admission to inpatient rehabilitation was comparable, and functional gains during inpatient rehabilitation were similar between groups. More children with nonabusive than with abusive head trauma attained independent ambulation and expressive language after discharge from rehabilitation; the difference was no longer significant when only children aged >12 months at injury were examined. There was variability in delay to obtain these skills and in the quality of gained skills in both groups. Conclusions Despite more associated injuries, children with abusive head trauma make significant functional gains during inpatient rehabilitation, comparable with an age- and sex-matched sample with nonabusive head trauma. Key functional skills may be gained by children in both groups following discharge from inpatient rehabilitation. (J Pediatr 2014;164:613-9).
A
busive head trauma is a common cause of pediatric traumatic brain injury (TBI).1 Compared with children with nonabusive head trauma, mortality and morbidity are consistently greater in children with abusive head trauma.2-4 Younger age at injury,5,6 more severe initial injuries,2,7-9 and higher rates of secondary injuries from hypoxia and/or ischemia2,8,10 may contribute to the worse outcomes observed after abusive head trauma. For survivors of abusive head trauma, the neurodevelopmental outcome is often considered to be globally poor, though closer examination reveals a range of outcomes, especially in functional skills. Barlow et al examined a number of outcome variables at follow-up (mean 59 months postinjury) in 25 children with abusive head trauma. Although 68% of the children had neurologic or cognitive abnormality at follow-up, 60% of children were reported to have normal functional mobility, and 64% had normal to mildly impaired speech and language function.11 On standardized testing evaluating neurocognitive development and adaptive behavior, Keenan et al demonstrated worse outcomes in children with abusive head trauma, who also accounted for a larger percentage of the reported clinical disabilities including speech delay or need for assistive mobility devices.4 Even though global outcome ratings are useful for broadly categorizing outcomes, they may not provide a clear picture of an individual’s functional skills. In discussions of prognosis after abusive head trauma, caregivers often ask questions about expectations for development of discrete skills that can improve quality of life, such as independent ambulation (IA) and expressive language (EL).
DFQ EL GCS IA ICP LOS TBI TTA WeeFIM
Developmental Functional Quotient Expressive language Glasgow Coma Scale Independent ambulation Intracranial pressure Length of stay in a rehabilitation facility Traumatic brain injury Time from injury to admission to inpatient rehabilitation (time of acute hospitalization) Functional Independence Measure for children
From the 1Kennedy Krieger Institute; Departments of 2 Neurology, 3Physical Medicine and Rehabilitation, and 4 Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD; 5VA Medical Center, Perry Point, MD; and 6Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD Funded by the Eunice Kennedy Shriver National Institute of Child Health and Development (K23HD061611 and T32HD007414-20). The authors declare no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2014 Mosby Inc. All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2013.10.075
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The need for inpatient rehabilitation is a marker for severity of injury, as it signifies the presence of substantial functional deficits at the end of the acute hospitalization. Interestingly, reports of the outcome of children with abusive head trauma admitted to inpatient rehabilitation are not available, though this is theoretically a group at high risk for poor outcomes. The purposes of this study were to compare clinical features of children with abusive head trauma admitted to an inpatient rehabilitation unit to ageand sex-matched children with nonabusive head trauma, to evaluate and compare functional changes during inpatient rehabilitation in children with abusive head trauma and nonabusive head trauma, and to evaluate and compare attainment of key skills (IA and EL) by children with abusive and nonabusive head trauma at discharge from inpatient rehabilitation and subsequent follow-up.
Methods This is a retrospective review of children with or without abusive head trauma receiving acute inpatient rehabilitation for brain injury at a single academically affiliated rehabilitation hospital from 1995-2012. The practice at this hospital is to admit children with even the lowest levels of function after acquired brain injury for the purpose of addressing goals such as caregiver training, tolerance to positioning, and management of irritability while observing for improvements in the child’s functional status. Children who had received inpatient rehabilitation at another facility prior to admission to this facility were not included. The Johns Hopkins Institutional Review Board granted approval for examination of data extracted from a clinical performance database and from review of medical records. Abusive Head Trauma Thirty-three patients with abusive head trauma were identified based on the International Classification of Diseases, Ninth Revision code 995 at the time of admission to inpatient rehabilitation. On record review, 28 of those patients had a diagnosis of abusive head trauma documented in acute care medical records (age range 2-51 months) and were included in analyses. A multidisciplinary child abuse team or maltreatment expert at a tertiary referral academic medical center confirmed the diagnosis of abusive head trauma in 19 children. For an additional 5 patients, the episode of abuse was either witnessed (2), the perpetrator confessed (2), or an arrest was made (1). The remaining 4 cases had a documented diagnosis of abusive head trauma, but the available medical records did not provide additional detail regarding how the diagnosis was reached. Nonabusive Head Trauma Age-matched patients with nonabusive TBI were identified by International Classification of Diseases, Ninth Revision code 854. Matches were chosen from admissions at any time from 1995-2012 based on closest matching age of injury 614
Vol. 164, No. 3 within 3 months. We additionally prioritized matches of the same sex and without weight-bearing restrictions from orthopedic injuries. Age-matched controls were available for 20 of the 28 patients with abusive head trauma (age range 2-53 months); there were no matches available for 7 of the 11 children with abusive head trauma at #9 months of age at injury. Of the 20 matched controls, 2 children had documented formal consultation by experts in abuse and maltreatment, who concluded that each injury was accidental. Three matches were of the opposite sex. One matched control had coexisting fractures but was cleared for full weight bearing 9 days after admission to rehabilitation (27 days prior to discharge). One potential match was excluded due to symptomatic late pseudoaneuryms thought to be unrelated to the injury. Mechanism of TBI among the matched controls was variable: 11 patients were involved in a motor vehicle accidents, and 7 of these patients were documented as properly restrained. Three children had a television fall on their head, and 1 was accidentally struck in the head with a horseshoe. Two children were struck by cars. The remaining 3 patients were involved in falls: one fall from a bed, another fall down concrete stairs, and a third fall from an approximately 12-foot-high window. Glasgow Coma Scale (GCS) was defined as the first documented GCS score.12 GCS was available for 19 of 28 patients with abusive head trauma and 18 of 20 patients with nonabusive head trauma. Significantly increased intracranial pressure (ICP) was defined as direct documentation of elevated ICP in those undergoing ICP monitoring, requirement for neurosurgical interventions to relieve increased ICP (craniotomy or craniectomy), or neuroimaging reports of cerebral herniation or extensive cerebral edema with midline shift. Placement of an ICP monitoring device alone was recorded but not included in this variable unless there was clear documentation of increased ICP. Neuroimaging findings were recorded from head computed tomography or brain magnetic resonance imaging reports or, if neuroimaging reports were unavailable (ie, for patients transferred from another institution), from documentation of results by a medical provider within admission or discharge records. All patients had head computed tomography results available, and brain magnetic resonance imaging reports were available for 18 children with abusive head trauma and 11 children with nonabusive head trauma. Presence was noted of subdural hematoma, epidural hematoma, subarachnoid hemorrhage, and intraparenchymal hemorrhage; the latter 3 were grouped as “other brain hemorrhage.” Presence of skull fracture was also noted. The following were considered risk factors for neurologic sequelae, which might affect the child’s outcome: acute cerebral infarction/ischemia as documented in neuroimaging reports or clinical records, cardiac arrest or apnea requiring intervention, and documentation of status epilepticus during the acute hospitalization. Retinal hemorrhage was evaluated by physician documentation of the presence or absence of unilateral or bilateral Risen et al
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March 2014 findings. Twenty-five of 28 children with abusive head trauma had ophthalmological reports. Of those with nonabusive head trauma, 8 children had documented ophthalmological evaluations, 5 to assess trauma-related conditions such as orbital roof fractures. Time from injury to admission to inpatient rehabilitation (time of acute hospitalization) (TTA) was calculated as the number of days from acute care admission to admission to inpatient rehabilitation. Length of stay in a rehabilitation facility (LOS) was defined as the number of days from inpatient rehabilitation admission to discharge. Functional Independence Measure for Children (WeeFIM) is an 18-item, performance-based instrument measuring functional skills in self-care, transportation/ locomotion, and communication/social domains. The WeeFIM provides an objective measure of a child’s functional abilities, grading performance on specific tasks on an ordinal scale of 1-7 reflecting increasing level of independence/reduced need for assistance. Full independence on all measures within the scale is expected by 7 years of age. Because the degree of independence on tasks is expected to depend on developmental age, WeeFIM scores are converted into a Developmental Functional Quotient (DFQ). WeeFIM DFQs describe a child’s functional skills as a percentage of those expected by age, based on a normative sample of WeeFIM scores.13-15 WeeFIM DFQs for self-care, mobility, cognition, and total function were collected as part of clinical care at admission to and discharge from rehabilitation. Given the limited WeeFIM skills evaluated during infancy, WeeFIM data were used only from children who were at least 1 year of age at the time of admission, yielding WeeFIM data for 17 of 28 patients with abusive head trauma and 16 of 20 patients with nonabusive head trauma. IA and EL were chosen as important qualitative functional outcomes. IA was defined as documentation of ambulation in daily living without assistance from another person. EL was defined as use of spoken words for communication. Documentation of IA and EL was available for all patients at discharge; however, at discharge, 11 patients in the abusive head trauma group and 4 patients in the nonabusive head trauma group were 12 months of age with abusive and nonabusive head trauma attained IA (59% vs 75%) and EL (59% vs 69%) by discharge from inpatient rehabilitation. Overall, 64% of children with abusive head trauma later gained IA, and a significantly higher percentage of children with nonabusive head trauma attained IA (95%) (P = .03). Ambulatory skills ranged from independent steps for inhome mobility to hemiplegic gait to age-appropriate community mobility and advanced gross motor skills. The median age of children who gained IA after discharge from rehabilitation was similar between groups (abusive head trauma: median age 26 months, range 14-30 months; nonabusive head trauma: median age 26 months, range 14-38 months). Additionally, IA was acquired, on average, 14 months after discharge (range 2-19 months) in children with abusive head trauma and 9 months (range 1-25 months) after discharge in the nonabusive head trauma cohort. Tables IV and V (available at www.jpeds.com) provide details on each patient including age at attainment of IA and EL and a description of function at the last available documentation (which ranged from the time of discharge to 16 years after discharge). EL skills ranged from single words used for basic communication to complete, fully articulated sentences and conversations. Although a higher percentage of children with nonabusive head trauma also attained EL (95%) compared with those with abusive head trauma (72%), this difference was not statistically significant (P = .11). EL was gained within a similar age range in both groups (abusive head trauma: median age 32.5 months, range 14-38 months; nonabusive head trauma: median age 26 months, range 14-48 months); Additionally, patients with abusive head trauma attained EL an average of 16 months after discharge from rehabilitation (range 7-31 months) compared with 7.4 months (range 1-25 months) in children with nonabusive head trauma. To evaluate the relationship between age at the time of injury and functional outcomes, group differences were examined in the subset of children aged $12 months at the
Table II. Change in mean WeeFIM DFQs from admission to discharge within and between groups* Abuse head trauma (n = 17)
Nonabusive head trauma (n = 16)
WeeFIM DFQ
Admission† DFQ
Dischargez DFQ
P value
Admission† DFQ
Discharge† DFQ
P value
Difference between groups over time, P value
Self-Care Mobility Communication Total
52 33 46 42
59 51 61 54
.053 .004 .016 .006
48 33 46 41
59 55 65 59
.007 .001 .001 .001
.355 .285 .267 .160
DFQ: (patient domain score/expected domain score per age) 100. *Children aged >12 months at the time of injury. †Difference in admission DFQs between groups is not statistically significant for any subset or total score. zDifference in discharge DFQs between groups is not statistically significant for any subset or total score.
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Table III. Attainment of IA and EL At discharge from rehabilitation (Excluding children aged £12 months at injury)
IA, No. EL, No.
Abusive head trauma (n = 17)
Nonabusive head trauma (n = 16)
P value
10 (59%) 10 (59%)
12 (75%) 11 (69%)
.47 .72
At follow-up evaluation* (Excluding children with insufficient follow-up documentation)
IA, No. EL, No.
Abusive head trauma (n = 25)
Nonabusive head trauma (n = 19)
16 (64%) 18 (72%)
18 (95%) 18 (95%)
.03 .11
At follow-up evaluation (Excluding children aged £12 months at injury and those with insufficient documentation) Abusive head trauma (n = 15)
Nonabusive head trauma (n = 16)
11 (73%) 13 (87%)
15 (94%) 15 (94%)
IA, No. EL, No.
.17 .60
*Age at which IA and EL gained, months to gain IA and EL, as well as descriptors of final outcome can be found in Tables IV and V.
time of injury, and there was no longer a significant betweengroup difference in attainment of IA (P = .17) or EL (P = .60). Furthermore, in examining overall functional outcomes independent of mechanism of injury, children who attained IA and EL were older at injury than were those who did not (P = .045 and P = .08, respectively). Children who experienced associated injuries were less likely to achieve IA (P = .027) than were those who did not have secondary neurological insults. No other demographic or injury related factors were related to follow-up outcome of IA or EL.
Discussion Children with abusive and nonabusive head trauma were similar with respect functional impairment at admission to inpatient rehabilitation and gains made during inpatient rehabilitation. This highlights the potential for children with abusive head trauma to make short-term functional gains and benefit from inpatient rehabilitation. The use of age- and sex-matched populations of children with abusive and nonabusive head trauma is important, as younger age at injury has been associated with worse neurodevelopmental outcome5,6 and sex may modify response to ischemic insults or brain injury.16,17 Although the groups were age matched overall, there were more children aged #9 months at injury within the abusive head trauma group, consistent with the higher rate of abusive head trauma in infants.18 The average age of children with abusive head trauma in our sample was 20 months, which is older than that in many prior reports.18,19 This may reflect our inclusion of children through 5 years of age and a bias toward fewer but more impaired infants in our inpatient rehabilitation sample, as infants with sufficient feedings skills are commonly discharged from acute care to a home setting. GCS scores and signs of increased ICP were similar between groups, reflecting similar injury acuity. Neuroimaging and retinal hemorrhage findings are consistent with current
understanding of abusive head trauma and suggest that our patients were appropriately categorized.20 Associated injuries with neurological impact were significantly more common in children with abusive head trauma; both ischemia/infarction and status epilepticus were 6 times more common in abusive head trauma, and cardiorespiratory arrest/apnea was 4 times more common in abusive head trauma. This is consistent with prior reports of ischemia/infarctions,8,10,21 cardiorespiratory arrest/apnea,2,22,23 and posttraumatic seizures6,24 occurring more frequently in abusive head trauma. Similar to prior reports correlating severity of injury with disability in children with TBI,2,4,19 the presence of associated injuries was associated with worse outcome in our sample. Distinguishing the independent contribution from mechanism and severity of injury on outcomes is difficult given the overlap in abusive head trauma and associated injuries. However, in our sample, there was no difference in TTA, indicating that duration of acute hospitalization was similar despite the increased associated injuries in children with abusive head trauma. Although not statistically significant, the longer LOS in rehabilitation for the children with abusive head trauma may reflect social factors associated with abusive head trauma, which can complicate discharge planning or may reflect that children with abusive head trauma need additional time to gain a similar degree of skills. Even though we were unable to examine quantitative functional gains during inpatient rehabilitation in children aged #12 months due to the lack of reliable standardized functional assessment tools for this population, we were able to assess the rate of achievement of IA and EL in children injured at all ages. More than 50% of children with abusive and nonabusive head trauma achieved these skills at the time of discharge from inpatient rehabilitation; as children admitted to inpatient rehabilitation typically do not have IA, this again highlights the opportunity for meaningful short-term functional gains from inpatient rehabilitation in children with brain injury.
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Almost all children with nonabusive head trauma attained IA and EL after discharge from inpatient rehabilitation, whereas two-thirds of children in the abusive head trauma group eventually gained IA and nearly three-fourths gained EL within 31 months from rehabilitation discharge. The discrepancy in functional outcomes between children with abusive and nonabusive head trauma has been previously reported in a younger cohort of children.2,4,8 Although the abilities to ambulate and communicate have important implications for a child and the family’s daily function, the quality of these skills was variable in this cohort. It is also important to note that children in both groups achieved IA and EL well beyond the developmentally expected age range and often >12 months from the time of discharge. This is consistent with prior reports of children attaining functional skills over several years after TBI.25 When our analysis of IA and EL was limited to children at least 12 months of age at injury, there was no longer a significant difference in between-group outcome at follow-up. This is consistent with prior studies identifying worse outcomes in younger children with TBI,5,6 though other studies have failed to find differences in outcome based on age.25-27 This finding may also reflect the bias of our sample toward the most impaired infants. Larger studies with a matched sample of the youngest children would be useful for assessing differences in outcomes for infants with TBI. Additional limitations of this study include small sample size with documentation ranging over a 17-year period from multiple providers although drawn from a single rehabilitation unit; even though this was necessary to achieve the relatively small sample size presented, it is possible that variations in care during that period could have influenced outcomes. As admission practices vary among rehabilitation institutes, our cohort may differ from those admitted for inpatient rehabilitation elsewhere. Although WeeFIM data represent quantitative data acquired prospectively as part of clinical care, the other data obtained through chart review are based on documentation that was occasionally incomplete. For instance, we were unable to evaluate long-term outcomes in cognition and behavior due to inconsistent documentation of these skills in the available records. We were also unable to gather complete data on family and socioeconomic factors that have also been shown to influence outcome after TBI in children.4,28 Future studies designed to prospectively collect outcome data in a standardized fashion across multiple centers would be useful for better understanding the range of outcomes after abusive head trauma. Combining such outcome data with updated acute evaluations, such as biological markers and advanced neuroimaging techniques, will be useful for improving prognostication shortly after injury. n Submitted for publication May 29, 2013; last revision received Sep 19, 2013; accepted Oct 28, 2013. Reprint requests: Stacy J. Suskauer, MD, 707 N Broadway, Baltimore, MD 21230. E-mail: [email protected]
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